Disorders of Higher Motor

Control

Raffaella Ida Rumiati

Scuola Internazionale Superiore di

Studi Avanzati

Trieste, Italy

rumiati@sissa.it

The term apraxia

• has been used in 1881 for the first time by Heymann Steinthal.

• He described an aphasic patient who grasped the pen upside down when trying to write and manipulated the knife as a fork.

• Steinthal proposed that the locus of the problem was between the movements and the objects to be manipulated.

Asymbolia

• Finkelburg (1870) had argued that apraxic and aphasic disturbances have a common cause and used the concept of asymbolia to describe this condition.

• But Steinthal distinguished apraxia from asymboliabecause the former concerns not only meaningful signs but also concrete objects.

• The fact that aphasia and apraxia have later been shown in double dissociation invalidates the asymbolic argument.

Clinical Definition

• Apraxia refers to a deficit of the motor activity that emerges

specifically during the execution of intentional actions.

• It is not due to:

• deafness or aphasia

• primary sensory weakness (blindness or tactile anesthesia)

or agnosia (visual or tactile)

• paresis, tremor, ataxia, ipokinesis (Parkinson) or iperkinesis

(Còrea)

• impaired spatial orientation

• impaired body schema

• frontal inertia or dementia

Clinical classifications

• Apraxias are classified according to the

body segment that is involved:

– Bucco-facial apraxia

– Trunk apraxia

– Limb apraxia

• The fact that the apraxic deficit can affect

one body part at the time speaks against

the asymblolic account of this disorder.

Bucco-Facial Apraxia• This affects the muscles of mouth, tongue, pharynx and

larynx.

• Patients with BFA have difficulties in protruding the tongue, whistling, protruding the lips (kissing), swallowing etc.

• This can be observed either when the P is requested to do it verbally by the examiner or when P is asked to copy what the experimenter does.

• The same movements that the P cannot perform when requested can be executed spontaneously in other circumstances (voluntary-automatic dissociation).

• It is often associated with speech apraxia (or anarthria)because of the anatomical contiguity of the areas involved, however double dissociations between the two have been also reported.

• ABF is caused by lesions of the anterior insula in the left hemisphere.

Trunk Apraxia• Geschwind suggested a possible dissociation

between limb movements and those that executed by the axial musculature (e.g. trunk), preserved in patients with limb apraxia.

• Afterwards, dissociations between axial movements and movements performed by other body parts have been confirmed but only on verbal command.

• Yet other studies failed to observe spared performance of axial movements, thus weakening the Geschwind’s hypothesis.

• Trunk apraxia is associated with bilateral frontal lesions that can also cause gate apraxia.

Limb Apraxia

• In right handed patients, a lesion of the left hemisphere can produce apraxia of both upper limbs.

• The movements of the lower limbs can be affected too, but they are only rarely tested.

• The upper limb tested is normally the one ispilateral to the lesion.

Clinical classification based on the

function affected

• Following the model of Liepmann that I will now present, apraxias can be distinguished depending on which function (task) is reduced in the patient.

Liepmann

• In 1900 he published a detailed single case report of a left handed patient (Regierungsret) afflicted by syphilis who had apraxia when he performed an imitation task with the left but not the right hand.

• The autopsy revealed that 2/3 of the CC were completely destroyed, and subcortical cysts in the left frontal and parietal lobes interrupted most of the remaining connections between the left central region and other cortical regions (callosal apraxia).

• In 1905, Liepmann observed 20/41 patients with right hemiplegia and apraxia, and 42 patients with left hemiplegia non of whom had apraxia thus establishing that the left hemisphere was specialized for motor control.

Ideational Apraxia

• At the basis of a purposeful action there is a movement formula.

• This is a visual or acoustic image of an action and not a kinetic memory.

• The MF is the product of the entire cortex but the posterior regions may play a critical role when the MF is provided by a visual image.

• A failure to create an appropriate MF leads to IdeationalApraxia.

• According to Liepmann, IA is mainly caused by diffuse brain lesions and dementia.

• He did, however, consider the possibility that occipito-parietal lesions might cause IA.

Ideomotor Apraxia (AIM)• The 2nd step from intention to action requires

connecting the movement formula to the motor innervations.

• Failure to this mechanism leads to IdeomotorApraxia (motor or ideo-kinetic apraxia).

• It can be evidenced by faulty imitation of movements.

• It does not affect routine actions (i.e. knocking the door).

• IMA is caused by interruption of fibers from the whole cerebral cortex to the motor center for the affected limb.

Limb-kinetic apraxia

• Loss of purely cinematic memories of an

extremity leads to LKA.

• This form of apraxia affects purposeful as

well as routine use of objects.

• LKA results from lesions to the central

region.

Clinical classification based on the

function affected

• IMA

• IA

• LKA

Disconnection Account of Apraxia

• Failure to gesture to verbal command (or imitation):

– The verbal command is processed in the Wernicke area, and from here the info is sent to the ipsilateral premotorcortex, through the fasciculum arcuatum.

– To move the R hand, the info needs to be sent from the left PMC to the left M1;

– to move the L hand, the info needs to be sent, through the CC, from the left to the right PMC, that in turn projects to the right M1.

– Lesions of the left posterior parietal cortex in the LH disconnect the Wernicke’s area (or the visual associative cortex) from the PMC, thus preventing the verbal command (or visual stimulus) to be executed.

Geschwind 1965, Disconnection syndromes in animals and man

Rothi et al. (1991)

• proposed a model of comprehension (input) and

of production (output) of actions inspired to

models of language production.

• Such model can explain a number of

phenomena:

• Input/output dissociation

• modality-specific apraxias (e.g.verbal/visual)

• Imitation of meaningless actions

SEMANTIC

MEMORY

MOTOR OUTPUT

ACTION

VISUAL

ANALYSIS

BUFFER

ACTION OUTPUT

LEXICON

AUDITORY

ANALYSIS

SPOKEN WORD

PHONOLOGICAL

lNPUT LEXICON

PHONOLOGICAL

OUTPUT LEXICON

BUFFER

NAMING

VISUAL

ANALYSIS

OBJECT

SDS ACTION INPUT

LEXICON

TESTING A COGNITIVE MODEL OF

PRAXIS

• IMA

– IMITATION (MF-ML)

– PANTOMIMING TO VERBAL COMMAND

– PANTOMIMING SEEN OBJECTS

• IA

– OBJECT USE

SEMANTIC

MEMORY

MOTOR OUTPUT

ACTION

VISUAL

ANALYSIS

BUFFER

ACTION INPUT

LEXICON

Imitation of ML actions

Imitation of MF actions

ACTION OUTPUT

LEXICON

Participants

• Stimuli & Task

– Imitation of 20 MF & 20 ML actions

• Procedure

– mixed and separate lists in 2 different days.

• Hands

– examiner/right

– patients/ipsilateral to the lesion.

• Accuracy & Error analysis

Stimuli & Procedure

Single Case AnalysisMixed Lists

• None of the patients showed a dissociation in imitation of

mixed MF and ML actions.

• In the mixed condition, patients select the sub-lexical route

for imitating both MF and ML actions.

• As the brain damage reduces the patients’ resources, the

sub-lexical route is selected because it allows to reproduce

both action types.

• If the route is damaged, imitation of both MF and ML actions

may result impaired.

• The same findings have been reported by De Renzi et al.

(1980), Cubelli et al. (2000) and Toraldo et al. (2001) where

a mixed list was employed.

Blocked Lists

MF > ML ML > MF

Action recognition (C 31 = 100% and C 30 = 95%)

0

5

10

15

20

C 2 C 6 C 19 C 13 C 14 C 23 Ctrls C30 C31

RBD LBD LBD

subjects

# correct responses

MF

ML

SEMANTIC

MEMORY

MOTOR OUTPUT

ACTION

VISUAL

ANALYSIS

BUFFER

ACTION OUTPUT

LEXICON

ACTION INPUT

LEXICON

Deficit in imitation

of MF actions

xx

Deficit in imitation

of ML actionsStrategic control

Two imitation routes & strategic control

• When MF and ML actions are presented in

separate blocks, patients select the route

depending on the stimulus type.

• Depending on which route is damaged,

patients show a selective deficit in imitation of

either MF or ML actions.

• Patients with selective imitation deficits have

been reported before:

– Goldenberg & Hagmann 1997; Peigneux et al.

2000; Bartolo et al. 2001.

IMPAIRED IMITATION OF ML ACTIONS

Patients LK EN

ML hand positions 11/20* 3/20*

ML finger configurations 19/20 11/20*

PRESERVED IMITATION OF MF ACTIONS

LK EN

Pantomimes of object use 17/20 18/20

IMPAIRED IMITATION OF ML POSITIONS

LK EN

ML hand positions on mannikin 10/20* 5/20*

IMA & BODY SCHEMA

Goldenberg & Hagmann 1997

SEMANTIC

MEMORY

MOTOR OUTPUT

ACTION

VISUAL

ANALYSIS

BUFFER

ACTION OUTPUT

LEXICON

ACTION INPUT

LEXICON

Deficit in imitation

of MF actions

xx

Deficit in imitation

of ML actions

Body

Representationx

• In 3 experiments, we investigated:

– the existence of these two putative processes for action reproduction

– whether they can be strategically selected to achieve the best performance depending on:

• type of stimulus (MF-ML)

• composition of the list (blocked-mixed)

• information about the experiment list

• relative proportion of the two stimulus types.

Events in a Trial

empty screen

250 ms

Response window

500 ms

250 ms

deadlinetime

1 sec.

Without time constrains, subjects perform at ceiling.

Methods

• 20x4 MF actions = pantomimes of object use

• 20x4 ML actions = as MF but not recognized.

• The model demonstrates the action with the left

hand (movie).

• Subjects execute it with the right hand.

• Imitation performance was video-recorded and later

scored by 2 independent raters.

• Two dependent variables: Accuracy and Errors.

• Blocked : Experiment 2A > Experiment 1A (p < .05)

• Mixed : Experiment 1B > Experiment 2B (p < .05)

Experiments 1 (without) & 2 (with)

AIM anatomy

• Lesion studies addressing the question of the

anatomical basis of IMA failed to unveil the specific

lesion correlating with this form of apraxia.

• It is most frequently associated with LH brain-

damage, though there have been a few patients

with apraxia as a result of a RH or subcortical

lesion (Basso et al. 1980; De Renzi et al. 1982).

• Critical areas are: left parietal and premotor cortex.

SEMANTIC

MEMORY

MOTOR OUTPUT

ACTION

VISUAL

ANALYSIS

BUFFER

ACTION OUTPUT

LEXICON

AUDITORY

ANALYSIS

SPOKEN WORD

PHONOLOGICAL

lNPUT LEXICON

PHONOLOGICAL

OUTPUT LEXICON

BUFFER

NAMING

VISUAL

ANALYSIS

OBJECT

SDS ACTION INPUT

LEXICON

Ideational Apraxia• Humans skilfully use a very large range of objects by

making a series of object-specific movements.

• After LBD, however, right-handers may experience a reduced ability to use objects and tools in everyday life.

• This failure to use common objects and tools is a key symptom of IA.

• Early reports of this deficit describe patients trying to use a pair of scissors as a spoon or taking the wrong side of a smoking pipe to the mouth (Pick).

• IA has been observed in patients without IMA, defined as a failure to imitate actions, and vice versa (e.g. De Renzi et al. 1968; De Renzi & Lucchelli,1988; Ochipa et al.,1992).

• This suggests that IA cannot simply be a more severe instance of IMA.

De Renzi et al. 1965

3411I A +

11104I A -

I M A +I M A -(n = 160)

• Actual use of common objects in isolation or in a context.

• Poeck argued that IA can be observed only when objects are used in a complex context.

• De Renzi & Lucchelli (1988) showed a strong correlation between single tool use and use of objects in a complex context(e.g. lighting a candle).

Testing IA

IA AS A FAULTY

REPRESENTATION OF THE

SEQUENCE

• LH brain-damaged patients were reported

with an impairment in performing everyday

actions as well as in sequencing photographs

depicting those actions (Poeck).

• According to this view, IA arises from a

representational damage to the sequential

organization of actions with objects.

• De Renzi & Lucchelli proposed that IA

is due to a difficulty in accessing the

semantic repertoire of functional

features of objects.

• However these authors did not test

patients’ semantics and visual

processing.

IA as amnesia of obejct use

PATIENTS

DR• no visual agnosia• no memory deficits• Broca’s aphasia with

mild comprehension problems

FG• no visual agnosia, STM

but not LTM memory deficits, normal language production and comprehension.

Assessment of praxic abilities

FG DR

Imitation 50/72 34/72 cut off < 53-62

57/72 43/72

Real use 4/14 6/14 cut-off < 14

13/14 8/14 cut-off < 14

Pantomime 16/28 6/28 mean 20.20±2.93

Conceptual Errors

Mislocation of an action (II)

• FG often (18.5%) selected the correct target-object on which to operate with an instrument-object in hand but got the exact location wrong:– e.g. striking a match inside the matchbox

Object Misuse (II)

• DR often (40%) selected an appropriate action to the object in hand but inappropriate to the context:– e.g. pressing the knife on an orange rather than

performing a sawing movement

NO Visual AgnosiaDRDR FGFG

Object identification 100% 100%

Action identification 100% 100%

NO Loss of functional-semantic knowledge

Function-to-object match (out of 4) 100% 100%

Object-to-function match (out of 3) 100% 100%

SEMANTIC

MEMORY

MOTOR OUTPUT

ACTION

VISUAL

ANALYSIS

BUFFER

ACTION OUTPUT

LEXICON

AUDITORY

ANALYSIS

SPOKEN WORD

PHONOLOGICAL

lNPUT LEXICON

PHONOLOGICAL

OUTPUT LEXICON

BUFFER

NAMING

TACTILE-VISUAL

ANALYSIS

OBJECT

SDS ACTION INPUT

LEXICON

• We suggested that IA in DR and FG was caused by a faulty functioning of the Contention Scheduling.

• The CS is competition mechanism that allows routine actions to be produced without conflict

• It does so by activating relevant and inhibiting irrelevant action schemata at appropriate times set by environmental triggers.

• In particular, IA in DR and FG can be interpreted as a damage to, or a disconnection between, components within the CS such as the object-trigger system and the action schemata.

• In a follow-up study we investigated whether FG’s and DR’s failure to use objects was determined by a loss of finer functional knowledge of parts of objects.

• Moreover we aimed at demonstrating that object use is not dependent upon declarative, functional-semantic knowledge.

• We therefore compared performance of the apraxic patients with that of DL and AM with a semantic deficit, on a number of key tests.

Rumiati et al. (in prep.)

Probable DATProbable SDAetiology

femalemaleGender

rightrightHandedness

76 yrs71 yrsAge

5 yrs5 yrsEducation

AMDL

Patients with a semantic deficit

• Omissions and semantic paraphasias in naming and spontaneus speech;

• Semantic loss – word-picture matching tasks – associative matching tasks (pict. & words)

• Amnesia (words & faces)

• Spared Repetition

Neither apraxia nor agnosia!

Diagnosis of SD

• Both DL and AM had Left-Temporal

Atrophy as shown by:

– 1999 CT-scan negative

– 2000, 2002 SPECT: lower concentration of

the marker in the left temporal lobe.

• DL suffered from Semantic Dementia, and

AM, from DAT.

Battery of 22 objects

• General semantics

• Functional semantics of parts

• Object use

• Object & action recognition

Questionnaire

HAMMER1. supraordinate info: is it an object, a vegetable or an

animal?

2. category info: is it a tool, a musical instrument or a gem?

3. subordinate perceptual info: is it made of glass, of metal or of cement?

4. subordinate structural info: is it smaller than a screw? (yes/no)

5. functional info: is it used for cutting, screwing or sticking nails?

6. the protypical user of the object: is it used by the painter, the carpenter, the glazer?

Object Use vs. General Semantics

0

20

40

60

80

100

FG DR DL AM

% correct

Object Use Sem Pict Sem Words

N = 22

Functional semantics of parts

Which part is it used for lighting?

1. 2.

3. 4.

13.

Which part do you scratch?

1.

3.

2.

4.

Object Use vs. Semantics of Parts

0

20

40

60

80

100

FG DR DL AM

% correct

Object Use Sem Parts

N = 23

Summary

• Apraxic patients failed to use objects that

they could identify without hesitation in a

word-to-object matching test.

• Of these objects, FG and DR retained:

– semantic and functional knowledge

– functional knowledge of an object’s parts

Negri et al. 2007

Object Use

0

20

40

60

80

100

DL AM

Pat ient s

2002

2004

nsns

Object Use & Semantics

Object Use

AM DL

General Semantics/words

Conclusions

• The tests used contacted patients’ semantic properties and motor-based properties:

– semantic-functional properties are affected in DL + AM

– motor-based properties are affected in FG + DR (output).

• We suggest that these two sets of properties are organised in modules of a distributed object representation.

Selection Process

Semantics

functional knowledgeAction schemas

ACTION OUTPUT

FG & DR

Environmentaltriggers

Object

trigger system

DL & AM

• These two subsets of properties are likely to

have different neural bases.

• Patients with a semantic deficit had an

atrophy of the left temporal lobe, whereas

the lesion of the apraxic patients overlapped

in the left inferior posterior cortex (BA 40).

Where in the brain?

• Neuropsychological attempts to analyse

the neural bases of skilful object use and

imitation have proved difficult because:

– patients tend to have rather large lesions and

additional deficits, e.g. action and object

agnosia, or deficit in action imitation.

– it is difficult to collect a large series of

patients with selective deficits.

• IA of both limbs can be observed after a

vascular lesion in the left-hemisphere of right-

handers suggesting that is a focal symptom.

• Liepmann (1900-1920) left occipito-parietal junction

• De Renzi & Lucchelli (1988) left temporo-parietal

junction

IA, 3

Stimulus

Objects Actions

Naming NO NA

Response

Imitation IO IA

• 14 male subjects (mean age 26.14 ± 6.05)

• right-handed

• 90 different videotaped actions/objects were showed on a screen installed ahead of the subjects in the PET-scanner

• 12 PET-scans with 3 repeats per condition were carried out for each subject

• For each rCBF measurement, subjects viewed a white screen for 15 sec, then the stimulus sequence for 90 sec (each trigger 2.5 sec plus 0.5 sec ISI)

• Subjects performed the production task using the right hand

Main effect: Response

Imitation > Naming

Naming > Imitation

Main effect: Stimulus

Action > Object

Object > Action

DLPFC

-48, +8, +44; T=5.46

AAC

-4, +30, +34; T=5.55

VLPFC

-44, +46, +6; T=6.46

d IPL

-52, -44, +46; T=5.19

v IPL

-58, -32, +30; T=5.30

Interaction

(IO - IA) - (NO - NA)

p ≤ .05

Conclusions

• Our findings suggest a close link between seen objects and the motor information associated with actual use.

• In right-handed individuals, the key brain structure for an object system that triggers actions is in the left dIPL (BA 40).

• This provides an explanation of why left parietal damage may result in impaired tool use despite preserved lexical and semantic knowledge.

SEMANTIC

MEMORY

MOTOR OUTPUT

BUFFER

ACTION OUTPUT

LEXICON

AUDITORY

ANALYSIS

SPOKEN WORD

PHONOLOGICAL

lNPUT LEXICON

Pantomiming to verbal command

SEMANTIC

MEMORY

MOTOR OUTPUT

BUFFER

ACTION OUTPUT

LEXICON

VISUAL

ANALYSIS

OBJECT

SDS

Pantomiming the use of seen objects